REVIEW ARTICLE/BRIEF REVIEW

Transesophageal lung ultrasonography: a novel technique forinvestigating hypoxemia

L’echographie transœsophagienne pulmonaire: une techniqueinnovante pour evaluer l’hypoxemie

Yiorgos Alexandros Cavayas, MD . Martin Girard, MD . Georges Desjardins, MD .

Andre Y. Denault, MD, PhD

Received: 29 February 2016 / Revised: 10 June 2016 / Accepted: 13 July 2016 / Published online: 29 July 2016

� Canadian Anesthesiologists’ Society 2016

Abstract

Background Acute deterioration in respiratory status

commonly occurs in patients who cannot be transported for

imaging studies, particularly during surgical procedures and

in critical care settings. Transthoracic lung ultrasonography

has been developed to allow rapid diagnosis of respiratory

conditions at the bedside. Nevertheless, the thorax is not

always accessible, especially in the perioperative setting.

Transesophageal lung ultrasonography (TELU) can be used

to circumvent this problem.

Purpose The aim of this narrative review is to provide a

complete description of the TELU technique by

summarizing the existing literature on the subject and

describing our own experience that extrapolates from

transthoracic lung ultrasonography.

Principal findings The use of TELU can provide point-of-

care real-time information for quickly establishing the

etiology of acute hypoxemia. The transesophageal probe is

placed in close proximity to the posterior regions of the

lungs where lung consolidation and pleural effusions are

most often seen; however, most of the artefacts relied on by

transthoracic ultrasound have yet to be validated with

TELU. Moreover, the relative invasiveness of TELU

compared with transthoracic ultrasonography may limit

its use to specific situations when the probe is already in

place, as during cardiac anesthesia or when the anterior

thorax is inaccessible. The main advantage of TELU may

lie in the ability to integrate both cardiac and pulmonary

assessments in one single examination.

Conclusion Anesthesiologists and intensivists who already

use transesophageal echocardiography on a regular basis

should consider adding TELU to their clinical assessment

of hypoxemia and related pulmonary pathologies.

Nevertheless, the literature specifically supporting TELU

is relatively limited, and further validation studies are

needed.

Resume

Contexte Des deteriorations aigues de l’etat respiratoire

de patients qui ne peuvent etre transportes pour des

examens d’imagerie sont frequentes, particulierement lors

d’interventions chirurgicales ainsi que dans le contexte des

soins intensifs. L’echographie pulmonaire transthoracique

a ete mise au point afin de permettre de diagnostiquer

rapidement la cause d’une deterioration respiratoire au

chevet du patient. Or, le thorax n’est pas toujours

accessible, particulierement dans un contexte

perioperatoire. L’echographie transœsophagienne

pulmonaire (ETOP) peut alors etre utilisee pour pallier

ce probleme.

This article is accompanied by an editorial. Please see Can J Anesth

2016; 63: this issue.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s12630-016-0702-2) contains supplementarymaterial, which is available to authorized users.

Y. A. Cavayas, MD � M. Girard, MD � G. Desjardins, MD �A. Y. Denault, MD, PhD

Universite de Montreal, Montreal, QC, Canada

M. Girard, MD � A. Y. Denault, MD, PhD

Centre Hospitalier de l’Universite de Montreal, Montreal, QC,

Canada

G. Desjardins, MD � A. Y. Denault, MD, PhD (&)

Institut de Cardiologie de Montreal, 5000 rue Belanger,

Montreal, QC, Canada

e-mail: andre.denault@umontreal.ca

123

Can J Anesth/J Can Anesth (2016) 63:1266–1276

DOI 10.1007/s12630-016-0702-2

Objectif L’objectif de ce compte rendu narratif est de

proposer une description complete de la technique d’ETOP

en resumant la litterature existante sur le sujet et en

decrivant notre experience, qui extrapole de la litterature

portant sur l’echographie transthoracique.

Constatations principales L’utilisation de l’ETOP permet

d’obtenir des informations au chevet en temps reel afin

d’etablir rapidement l’etiologie de l’hypoxemie aigue. La

sonde transœsophagienne est situee a proximite des

regions posterieures des poumons, ou les consolidations

pulmonaires et les epanchements pleuraux sont les plus

souvent observes. Toutefois, la plupart des artefacts sur

lesquels s’appuie l’echographie transthoracique doivent

encore etre valides pour l’ETOP. De plus, le cote

relativement invasif de l’ETOP, comparativement a

l’echographie transthoracique, pourrait limiter son

utilisation a des situations particulieres dans lesquelles

la sonde est deja en place, comme c’est le cas en anesthesie

cardiaque ou lorsque le thorax anterieur est inaccessible.

L’avantage principal de l’ETOP pourrait resider dans sa

capacite a integrer les evaluations cardiaques et

pulmonaires en un seul examen.

Conclusion Les anesthesiologistes et les intensivistes qui

utilisent deja l’echocardiographie transœsophagienne de

facon reguliere devraient envisager d’ajouter l’ETOP a

leur evaluation clinique de l’hypoxemie et des pathologies

pulmonaires associees. Toutefois, la litterature appuyant

specifiquement l’ETOP etant relativement limitee,

davantage d’etudes de validation sont necessaires.

Acute deterioration in respiratory status commonly occurs

in patients who cannot be transported for imaging studies,

particularly during surgical procedures and in critical care

settings. Accordingly, bedside assessment using

transthoracic lung ultrasonography was developed to

allow for rapid diagnosis of respiratory conditions at the

bedside, and there has been a growing interest in this new

imaging technique.1 International consensus

recommendations have been published to guide clinicians

in the use of ultrasound (US) to evaluate the lung.2

Nevertheless, the thorax is not always directly accessible

for conventional transthoracic ultrasonography, especially

in the perioperative setting. To circumvent this problem,

transesophageal windows can be used to image the lung in

an analogous manner to direct transthoracic approaches.

Few reports have been published addressing the specific

aspects of transesophageal lung ultrasonography

(TELU).3-15

The aim of this narrative review is to provide a

comprehensive description of the TELU technique by

summarizing the existing literature on the subject and

describing our own experience that extrapolates from the

transthoracic lung ultrasonography literature. In order to

identify pertinent literature published on TELU, we

searched PubMed, Google Scholar, and EMBASETM to

find relevant articles using multiple research strategies,

including a combination of [‘‘ultrasonography’’ or

‘‘transesophageal echocardiography’’] and [‘‘lung’’, ‘‘lung

diseases’’, ‘‘pleural effusion’’, ‘‘pneumonia’’,

‘‘pneumothorax’’, ‘‘consolidation’’, or ‘‘atelectasis’’] or

specific lung ultrasonography terminology such as ‘‘B-

lines’’, ‘‘Lung Rockets’’, ‘‘Lung Sliding’’. We used Web of

Science� for backward and forward citation tracking of

selected articles.

Indications and contraindications

The main indication for TELU is the evaluation of acute

hypoxemia in patients in settings where transthoracic

ultrasonography or other bedside imaging techniques are

either suboptimal or not available. Notably, it can be used

in any setting where a transesophageal echocardiography

(TEE) probe is already in place. These situations include

the intraoperative setting or when patients present with

conditions that might limit conventional transthoracic lung

US imaging, including morbid obesity, significant

subcutaneous emphysema, thoracic burns, or the presence

of other thoracic wounds or dressings (Table 1).

Transesophageal lung ultrasonography shares the same

contraindications and complications of TEE that have

already been extensively reported.16

Physics principles underlying lung US

Transthoracic lung ultrasonography relies not only on

accurate images of true lung tissues but also on the careful

interpretation of artefacts. These artefacts usually originate

at the pleural interface and thus are more difficult to

appreciate with TELU than with the transthoracic

approach. Indeed, with the close proximity of the pleura

to the esophagus, the probe provides a sectorial image with

poor resolution in the near field where the pleural line is

situated and where most artefacts are generated. Moreover,

as we discuss later in this article, it is unlikely that the

posteriorly generated artefacts of TELU can be used in the

same way as the anterior artefacts of the traditional

transthoracic US approach. As these artefacts can still be

observed with TELU, we will briefly review them in this

section, bearing in mind that their clinical utility has yet to

be evaluated.

Transesophageal lung ultrasonography 1267

123

‘‘Lung sliding’’ refers to the characteristic sliding

motion of the visceral and parietal pleura against each

other during movement of the lung with inflation and

deflation.17 ‘‘Lung pulse’’ represents smaller faster

rhythmic movements of the pleural interface synchronous

with the patient’s electrocardiographic tracing induced by

pulsatile blood flow through the pulmonary vessels.18 This

is best appreciated during periods of apnea. Lung sliding

and lung pulse of the left posterior lung can be observed

most easily in a longitudinal plane of the descending aorta

adjacent to the lateral aortic wall. ‘‘A-lines’’ are normal

horizontal repetitions of the pleural line generated by

reverberation19 (Fig. 1). Indeed, when the US beam

reaches the pleural interface, it is completely reflected

back towards the probe because of the strong acoustic

impedance of the air contained in the lung. The probe

captures most of the returning US, but part of it is also

reflected back towards the probe-patient interface. This

residual US beam is again reflected by the pleural interface,

which generates another, albeit weaker, artefactual pleural

line called ‘‘A-line’’. As the time delay between US

emission and reception is used to determine a structure’s

depth, the distance between each reverberation line will be

equal to the distance between the probe and the first pleural

line.

In contrast, ‘‘B-lines’’,19 also known as ‘‘comet tails’’ or

‘‘lung rockets’’, appear as shiny vertical lines that arise

from the pleural interface and move along with the

parenchymal pleura throughout the respiratory cycle

(Fig. 2). It is thought that they result from an increased

lung density that in essence allows US to penetrate the

visceral pleura. This may happen with decreased lung

aeration (atelectasis) or increased interstitial fluid

(pulmonary edema) or tissue (pulmonary fibrosis). In its

most extreme form, the complete de-aeration of lung

parenchyma allows imaging of true lung tissue, which

sports a liver-like echotexture. Nevertheless, a focal area of

increased lung density surrounded by residual air will

allow the US beam to self-propagate and generate multiple

successive reflections, resulting in hyperechoic laser-like

vertical lines originating from the visceral pleura and

extending all the way down the US field. The B-lines erase

all other images in the US field and do not fade. Z-lines are

also hyperechoic vertical lines, but they do not erase other

artefacts and tend to fade gradually. Their origin is not

completely understood. They are thought to be a normal

finding and do not have any known clinical utility. With

TELU, we look at the posterior lung zones where lung

density is often increased as a result of decreased aeration

Fig. 1 A-lines. ‘‘A-lines’’ are normal horizontal regularly spaced

repetitions of the pleural interface generated by reverberation. The 3D

lung model was generated using a Vimedix Simulator (CAE

Healthcare, Montreal, QC, Canada) with the permission of CAE

Healthcare

Fig. 2 B-lines. ‘‘B-lines’’ are shiny vertical lines arising from the

pleural interface

Table 1 Indications for TELU in the OR and the ICU

Indications

Differential diagnosis of acute hypoxemia (see Table 4)

Differential diagnosis of decreased respiratory system compliance

Qualitative and quantitative assessment of suspected pleural effusion

Monitoring the effects of ventilator settings and prone position in

ARDS

Monitoring extravascular lung water to guide fluid/diuretic therapy

ARDS = acute respiratory distress syndrome; ICU = intensive care

unit; OR = operating room; TELU = transesophageal lung

ultrasonography

1268 Y. A. Cavayas et al.

123

in supine mechanically ventilated patients. Thus, B-lines

should not be interpreted automatically as extravascular

lung water (Table 2).

Ultrasonographic diagnosis of specific lung pathologies

Pleural effusions

Rapid diagnosis of pleural fluid collections (effusions) in

the operating room (OR) and in the intensive care unit

(ICU) can be life-saving, as in the case of massive

hemothorax.10 Ultrasonography is a quick and sensitive

tool to detect the presence of pleural fluid at the bedside,

but it also allows for a thorough qualitative and semi-

quantitative assessment. Effusions make surrounding

structures, such as the ribs and the diaphragm, visible.

Moreover, the passively de-aerated lung may be seen

‘‘moving freely’’ in the effusion, resulting in what is known

as ‘‘lung flapping’’ or the ‘‘jellyfish sign’’ (Video 1,

available as Electronic Supplementary Material).20 Pleural

fluid should be carefully differentiated from ascites by

locating the diaphragm, liver, and spleen and from

pericardial effusion by locating the pericardium and

descending aorta. The reported sensitivity of TELU for

the detection of a pleural effusion is 97% and the

specificity is 100% using computed tomography (CT) as

a gold standard.7 The median volume at which an effusion

becomes detectable is 125 mL on the left and 225 mL on

the right.11 The aorta offers a convenient acoustic window

that greatly facilitates the visualization of left-sided

pathologies. Right-sided pathologies, on the other hand,

are always more difficult to detect. This is due to the

position of the esophagus which lies slightly on the left side

of the vertebral column. This results in an acoustic shadow

created by the vertebral bodies, thus preventing the US

beam from reaching the more posterior portion of the right

lung. In our experience, right-sided effusions as large as

300 mL have been completely missed.

Effusions should be qualitatively characterized as

simple or complex.20 Simple effusions appear as

anechoic and homogeneous free-flowing fluid (Fig. 3).

Complex effusions are more heterogeneous and may

exhibit various sonographic features such as septated

loculations (Fig. 4), gelatinous and tissue-like

echotexture, fibrin strands, and floating echogenic debris

(called the ‘‘plankton sign’’) (Video 2, available as

Electronic Supplementary Material). Simple effusions can

be transudates or exudates, but complex effusions should

be considered exudates unless proven otherwise.21

The clinical context is often most helpful in determining

the etiology of the effusion. It should also be pointed out

that the appearance of a hemothorax is highly variable.

Depending on the acuity of the hemothorax and whether

there was a preexisting pleural effusion, it may display a

Fig. 3 Simple effusion. Anechoic homogeneous free-flowing fluid in

the chest cavity

Table 2 Lung artefacts in transthoracic ultrasound

Artefact Description Diagnostic utility

Lung

sliding

Normal sliding motion of the visceral and parietal pleura against

each other with inflation and deflation of the lung

Absence associated with pneumothorax or selective intubation

Lung

pulse

Normal rhythmic movement of the pleural line induced by

pulsatile blood flow through the pulmonary vessels

Absence associated with pneumothorax

A-line Normal horizontal repetitions of the pleural line generated by

reverberation

Absent with lung consolidation

Erased by B-line

May be present with pneumothorax

B-line Abnormal shiny vertical line arising from the pleura, moving

along throughout the respiratory cycle. It erases other artefacts

and does not fade

May appear in processes associated with increased lung

parenchyma density, such as pulmonary edema, interstitial

diseases, and atelectasis

Z-line Normal hyperechoic vertical lines, but they do not erase other

artefacts and tend to fade gradually

No clinical utility

Transesophageal lung ultrasonography 1269

123

gelatinous tissue-like echotexture (clot), a heterogeneous

pattern with fibrin and debris, or even a relatively

hypoechoic and homogeneous aspect (Fig. 5). Effusions

with a tissue-like density may be difficult to differentiate

from consolidated lung. Colour Doppler may then be of

significant assistance by highlighting the blood vessels

contained in a consolidated lung in contrast with a

hemothorax where no blood vessels will be seen.

Finally, a semi-quantitative evaluation of the pleural

effusion can be carried out as it can have important

management implications. Many methods have been

proposed for this purpose.4,7,11,13,14 The most practical

approach, in our opinion, uses the maximal surface area of

the effusion on a transverse plane (CSAmax). At an

electronic multiplane angle of 0�, the effusion is scanned

up and down in order to find its maximal surface area,

which is usually located at a depth of about 30 cm from the

incisors. The image is frozen and the surface area is

measured by manually tracing its contour on screen

(Fig. 6). This procedure, by itself, can provide an

approximate estimate of the volume of the effusion

(Table 3).

For a more precise estimation, the axial length (AL) of

the effusion may be measured by subtracting the depth of

the probe at the proximal limit (Dproximal) of the effusion

from the depth of the distal limit (Ddistal).

AL ¼ Ddistal � Dproximal

The volume of the effusion (VE) is then estimated by

multiplying CSAmax by the AL.11

VE ¼ ALð Þ � CSAmaxð Þ

For example, an effusion seen from a depth of 30-45 cm

with a CSAmax of 35 cm2 would be estimated to contain

525 mL of fluid [i.e., (45-30) � 35].

Lung consolidation

Pneumonia, atelectasis, pulmonary contusion, neoplasm,

and pulmonary infarction all result in a similar pattern of

consolidation. The absence of alveolar air abolishes A-lines

and B-lines and produces a tissue-like echotexture,

sometimes called ‘‘hepatization’’ (Fig. 7). A sonographic

air bronchogram may be seen as hyperechoic bubbles

casting the bronchial tree (Fig. 8). When these bubbles

move to and fro with respiration, the phenomenon is called

a dynamic air bronchogram (Video 3, available as

Electronic Supplementary Material). It is a demonstration

of airway patency and thus rules out obstructive atelectasis.

In a transthoracic echocardiographic study, this sign was

shown to have a 94% specificity and a 97% positive

predictive value for the diagnosis of pneumonia, defined as

bronchoscopic confirmation of airway patency with

positive bronchoalveolar lavage specimens.22 Although

this study used a transthoracic approach, its findings likely

also apply to TELU. Nevertheless, it may be difficult to

distinguish pneumonia from atelectasis solely on the basis

of ultrasonographic findings as the dynamic air

bronchogram has poor sensitivity (61%). Compounding

the issue is the frequent occurrence of some degree of

atelectasis, which is an almost universal finding in patients

receiving mechanical ventilation. Once again, the clinical

context is the most useful element to establish a specific

etiology.

Ultrasonography may help to diagnose some

complications of pneumonia such as a parapneumonic

effusion, empyema, and lung abscess. Transesophageal

lung ultrasonography may also help to evaluate the extent

of atelectasis. The surface area of consolidation in the left

Fig. 5 Acute hemothorax. The texture of the fluid filling the chest

cavity is similar to that of the stagnant blood seen in the heart with

cardiac surgery during bypass

Fig. 4 Complex septated effusion. Fibrin strands attached to the lung

and the parietal pleura forming small pockets of fluid

1270 Y. A. Cavayas et al.

123

lung in the transverse plane as evaluated by TELU

correlated well with the area measured by CT.5,6,8 This

may help to optimize ventilation and oxygenation in

patients with acute respiratory distress syndrome (ARDS)

by quantifying lung recruitment with increasing positive

end-expiratory pressure (PEEP) (Fig. 9) and/or prone

positioning.

Alveolar-interstitial syndrome

The interstitial thickening produced by pulmonary edema

or fibrosis results in the appearance of vertical B-lines

described previously.23 (Fig. 2) In an acute setting,

pulmonary edema is almost always responsible for the

appearance of B-lines. This extravascular lung water

(EVLW) may be the product of increased hydrostatic

capillary pressure, as in left ventricular failure, or increased

capillary permeability, as in ARDS.20 Cardiogenic edema

usually results in a B-line distribution that is gravity

dependent, bilateral, and homogeneous. A noteworthy

exception is mitral regurgitation, which can be strikingly

localized, as an eccentric regurgitation jet can cause

selective congestion in the lung tissue corresponding to

the single pulmonary vein receiving the regurgitant jet.9 On

the other hand, ARDS is characterized by a patchy

distribution of B-lines and areas of reduced or absent

lung sliding.24 The number of B-lines seems to be

proportional to the amount of EVLW. Indeed, in an

animal model with acute lung injury induced by oleic acid,

a strong correlation was found between the number of B-

lines and the wet-to-dry ratio of the lung tissue.25 The B-

lines respond very quickly to changes in EVLW and thus

allow real-time follow-up of fluid or diuretic therapy.26 In

our experience, left-sided B-lines are present on the pre-

procedure TELU exam in a significant proportion of

cardiac surgery cases. While others have also reported the

presence of this artefact using TEE,15 the exact meaning of

Fig. 6 Cappers’s quantification method. At an electronic multiplane

angle of 0�, the effusion is scanned up and down in order to find its

maximal surface area, which is usually located at a depth of about 30

cm from the incisors. The image is frozen and the surface area is

measured by manually tracing its contour on screen (CSAmax). The

axial length (AL) is then measured by subtracting the depth of the

probe at the proximal limit (Dproximal) of the effusion from the depth

of the distal limit (Ddistal). The volume of the effusion is estimated by

the product of CSAmax and AL.11

Fig. 7 Lung hepatization. The absence of alveolar air abolishes A-

lines and B-lines and produces a tissue-like echotexture that

resembles that of a liver

Table 3 Simplified semi-quantification method for approximating

pleural effusion volumes

CSAmax Semi-quantitative size

\ 20 cm2 Small (\ 400 mL)

20-40 cm2 Moderate (400-1,200 mL)

[ 40 cm2 Large ([ 1,200 mL)

The volume of the effusion can be estimated from its maximal surface

area (CSAmax) in the transverse plane (0� electronic plane)

Adapted from Howard et al.13

Transesophageal lung ultrasonography 1271

123

their presence remains unknown. We should be cautious

before extrapolating the associations and scores described

with transthoracic imaging to TELU.

While the transthoracic approach allows interrogation of

a wide surface of the pleural interface, where B-lines

originate, the transesophageal approach allows

interrogation of only the pleura immediately apposed to

the posterior mediastinum. As there is often a gravitational

gradient in edema distribution, this could potentially render

TELU oversensitive. Further clouding the issue, atelectasis,

a common occurrence in the dependent lung zones of

patients under general anesthesia, has also been associated

with the presence of B-lines.

Pneumothorax

As air tends to accumulate in the non-dependent area of the

thorax, which is inaccessible to TELU in patients in the

supine position, it is highly unlikely that a transesophageal

approach could be of any diagnostic value for non-tension

pneumothorax. A speculative exception, however, might be

in patients in the prone position. Nevertheless, the cardiac

consequences of increased intrathoracic pressures, such as

collapse of the right atrium27 or diastolic obstruction of the

right ventricular outflow tract, may be observed. In

transthoracic imaging, a pneumothorax is characterized

by the absence of lung sliding, B-lines, and lung pulse.

Their absence has a 100% positive predictive value.28 The

identification of a net transition point between absent and

present lung sliding, termed ‘‘lung point’’, is

pathognomonic with a positive predictive value of

100%.29 None of these signs have been validated with

TELU, however, and future validation is unlikely.

Lung examination

Any standard 2-8 MHz multiplane transesophageal probe

can be used for TELU. Pending studies comparing

various imaging settings, we recommend using a

frequency of 4 MHz with no post-processing. Harmonic

imaging, automatic tissue optimization, and any other

form of post-processing should be turned off as they can

suppress the artefacts that are relied on for image

interpretation. The depth should be set at approximately

20 cm. We propose a systematic approach to the

examination as has been similarly established for

transthoracic lung US studies.2,30 We separate each

lung along the craniocaudal axis into apical, middle,

and basal regions. The origin of the left subclavian artery

is used as a landmark to identify the apical regions. The

superior pulmonary veins are used to mark the middle

regions. Finally, the inferior vena cava right atrial

Fig. 9 Lung recruitment with PEEP. Consolidations of the lung with air bronchogram are seen with PEEP of 10 but subsequently disappear as

PEEP is raised to 20. PEEP = positive end-expiratory pressure

Fig. 8 Air bronchogram. Hyperechoic air bubbles trapped in bronchi

are seen surrounded by lung consolidation

1272 Y. A. Cavayas et al.

123

junction is used to identify the basal regions. From each

of these landmarks identified at 0� on the multiplane

probe, a 90� electronic rotation of the transducer plane

allows for scanning the lungs in a longitudinal axis.

(Fig. 10A) From a cardiocentric starting position at

12:00, the TEE probe is rotated counter-clockwise to

examine the left lung, with continued rotation to examine

the right lung until a full rotation is completed. As

anatomical lung segments cannot be readily identified,

the position of the US beam is used to report our

findings as accurately as possible. To indicate the

position of the US beam, the position of the knob on

the handle of the probe is used as the hand of a clock.

The anterior region of the right lung is situated at 2:00,

the lateral at 3:00, and the posterior at 4:00. Similarly,

the anterior region of the left lung is at 10:00, the lateral

at 9:00, and the posterior at 8:00 (Fig. 10B; Video 4,

available as Electronic Supplementary Material).

Integrated cardiopulmonary approach to hypoxemia

and other common problems in the OR or ICU

The majority of episodes of hypoxemia are of primary

pulmonary etiology; however, the differential diagnosis

also includes various cardiac pathologies. Cardiogenic

pulmonary edema, secondary to left ventricular failure or

valvulopathy, and intracardiac or intrapulmonary shunt

may occur in some patients. Pulmonary embolism can also

be associated with severe hypoxemia. Whether with a

transthoracic or a transesophageal approach, the addition of

information gathered by TELU to the elements provided by

echocardiography allows a point-of-care integrated

approach to the acutely hypoxemic patient (Table 4). The

approach described in Table 4 reflects specific elements of

the literature as well as the experience of the authors. The

diagnostic accuracy, sensitivity, and specificity of TELUS

remain to be formally validated.

Fig. 10 TELU Examination

technique. (A) Lung zones in the

coronal plane. The origin of the

left subclavian artery is used as

a landmark to identify the apical

regions. The superior

pulmonary veins are used to

mark the middle regions. The

insertion of the inferior vena

cava in the right atrium is used

to identify the basal regions. (B)

Lung zones in the transverse

plane. The position of the knob

on the handle of the probe is

used as the hand of a clock in

order to indicate the position of

the ultrasound beam. The

anterior region of the right lung

is situated at 2:00, the lateral at

3:00 and the posterior at 4:00.

Similarly, the anterior region of

the left lung is at 10:00, the

lateral at 9:00 and the posterior

at 8:00. The 3D lung model was

generated using a Vimedix

Simulator (CAE Healthcare,

Montreal, QC, Canada) with the

permission of CAE Healthcare

Transesophageal lung ultrasonography 1273

123

Moreover, one can track the effect of specific ventilator

strategies on lung aeration31 while also looking at the

hemodynamic impact of this strategy, in real-time, at the

bedside. Carefully integrating lung aeration data with right

ventricular and left ventricular performance indicators may

help find the ‘‘sweet spot’’ in terms of PEEP settings,

especially in severe ARDS patients with cor pulmonale.

While assessment of lung aeration has been validated using

only a transthoracic approach, its principles should also

apply to TELU, albeit limited to the posterior lung zones.

Combined cardiopulmonary bedside ultrasonography

performed during the weaning process may help

differentiate between the multiple processes that hinder

weaning patients from mechanical ventilation.

Diaphragmatic dysfunction induced by mechanical

ventilation or iatrogenic phrenic nerve injury is an

underappreciated cause of weaning failure.32 Diminished

or paradoxical diaphragmatic motion may be observed

Table 4 Ultrasound-guided differential diagnosis of acute hypoxemia

Diagnosis Lungs Left Heart Right Heart

Pneumonia - Consolidation (unilateral[ bilateral)

- Dynamic air bronchogram

- Pleural effusion (simple or complex)

ipsilateral to consolidation

- Lung abscess

- Variable impact

- Reduced LVEF might be present

with septic cardiomyopathy

- Variable impact

- Reduced RVEF might be present

with septic cardiomyopathy

Obstructive atelectasis - Consolidation

- Early whole lung collapse may present

with absent lung sliding but preserved

lung pulse

- Absence of the dynamic air

bronchogram

- Usually normal

- Change in LAX position (horizontal

axis if left and vertical axis if right

atelectasis)

- Variable impact depending on the

degree of associated pulmonary

hypertension

Massive pleural

effusion with

compressive

atelectasis

- Massive pleural effusion

- Ipsilateral consolidation

- Usually normal - Normal

ARDS - Bilateral heterogeneously distributed

B-lines (‘‘skip areas’’)

- Focal areas of reduced or absent lung

sliding

- Posterior consolidation(s) unilateral or

bilateral

- Normal LV systolic and diastolic

function

- No valvulopathy

- Increased sPAP

- RV dilatation and hypokinesis

- IVC dilatation

Pneumothorax - Absence of lung sliding and pulse

- Absence of B-lines

- Presence of A-lines

- Lung point

- Small left cavities - Small right cavities

- IVC dilatation

- Inspiratory collapse of the right

atrium and/or the RVOT

Pulmonary embolism - In the acute setting, normal lung

examination

- May eventually develop pleural

effusion and/or area of consolidation

- Usually normal but D-shaped

interventricular septum if

associated with PH

- Increased sPAP

- RV dilatation

- McConnell’s sign

- IVC dilatation

- Thrombus in transit

Left ventricular failure - Bilateral homogeneously distributed B-

lines

- Simple bilateral pleural effusions

- Decreased LVEF

- Evidence of increased LA filling

pressures (E/e’)

- Variable impact

Left valvular pathology - Bilateral homogeneously distributed B-

lines

- Localized B-lines with eccentric MR

- Significant valvular pathology - Variable impact

ARDS = acute respiratory distress syndrome; E/e’ = ratio of the early transmitral filling (E) to the early mitral annular velocity (e’); IVC =

inferior vena cava; LA = left atrium; LAX = long axis; LV = left ventricle; LVEF = left ventricular ejection fraction; MR = mitral regurgitation;

PH = pulmonary hypertension; RV = right ventricle; RVEF = right ventricular ejection fraction; RVOT = right ventricular outflow tract; sPAP =

systolic pulmonary artery pressure

1274 Y. A. Cavayas et al.

123

easily with transthoracic US but less so with TELU.

Moreover, ultrasonography may allow clinicians to observe

de-recruitment with the lung aeration score, which is

derived from the presence of B-lines and atelectasis.33 A

complete description of the lung aeration score is beyond

the scope of this review as it was validated only with

transthoracic imaging. We refer the interested reader to the

excellent review by Bouhemad et al.30 Cardiogenic

pulmonary edema can also be responsible for

unsuccessful weaning. During the transition from positive

pressure ventilation to spontaneous unassisted breathing,

left ventricular diastolic dysfunction may be unmasked by

increased venous return,34 and systolic dysfunction may be

unmasked by increased left ventricular afterload.35

Ultrasonography can detect deterioration in systolic and

diastolic performance as well as the development of B-

lines. These processes are often overlooked but easily

treatable.

Finally, integrated cardiac and lung ultrasonography

could allow for more optimal fluid therapy in

hemodynamically unstable patients. The advent of

dynamic indicators has brought great improvement in the

ability to predict fluid responsiveness. Nevertheless, even

the most advanced echocardiographic parameters, such as

left ventricular outflow tract velocity time integral variation

with respiration or with passive leg raise, are not perfect.36

Absence of B-lines in the anterior thoracic cavity evaluated

with a transthoracic approach has been shown to be

associated with a normal pulmonary artery occlusion

pressure.19 In the context of fluid loading, a dynamic

increase in the number of B-lines is thought to represent

extravascular lung water and could be added as a safety

measure to limit volume expansion before overt pulmonary

edema becomes clinically apparent.37 This could be an

interesting avenue and should be evaluated prospectively.

Advantages and limitations

The main advantages of TELU include the ability to perform

the procedure at the bedside without the need to have access

to the patient’s chest, and it may provide real-time feedback

for interventions such as effusion drainage and fluid and

ventilation management. The probe is closely apposed to the

posterior regions of the lungs where pleural effusions,

consolidations, and B-lines primarily occur. This approach

allows access to the posterosuperior zones, considered

the blind spots of transthoracic ultrasonography created

by the scapulae.30 The main limitation of TELU is that it

has not yet been sufficiently validated. It is more invasive

than transthoracic ultrasonography and has significantly less

supporting evidence. Transesophageal lung ultrasonography

is also less sensitive to right-sided pathologies,11 and the

anterior and lateral aspects of the lungs are largely

inaccessible. Finally, TELU shares the main limitations of

transthoracic US, as it often relies on artefact interpretation

to gain insights into the lung and is clearly somewhat

dependent on the operator.

Conclusion

Transesophageal lung ultrasonography can provide point-

of-care real-time information about the presence of lung

consolidation, pleural effusions, and pulmonary edema.

Nevertheless, the major advantage of TELU lies in the

ability to integrate both cardiac and pulmonary assessments

in a single examination. Anesthesiologists and intensivists

who already use TEE on a regular basis should definitively

add this powerful tool to their clinical assessment. Though

a large body of evidence now supports transthoracic lung

ultrasonography, there are only few articles validating

TELU. Besides pleural effusion and posterior

consolidations, most of the approach presented in this

article relies on extrapolation from the transthoracic

literature and the authors’ experience. This calls not only

for studies validating specific aspects of this diagnostic tool

but also for broader studies evaluating the usefulness of

adding a lung evaluation component to TEE in various

settings.

Acknowledgements We sincerely thank Denis Babin and CAE

Healthcare for their help with the figures, and Antoinette Paolitto for

her help with the submission process.

Funding Support was provided solely from institutional and/or

department sources. Dr. Denault is supported by the Montreal Heart

Foundations and the Richard I. Kaufman Endowment Fund in

Anesthesia and Critical Care.

Conflicts of interest Dr. Denault and Dr. Desjardins are bedside

ultrasound instructors for CAE Healthcare. Dr. Girard is a consultant

for GE Healthcare.

Author contributions Yiorgos Alexandros Cavayas contributed

substantially to all aspects of this manuscript, including conception

and design; acquisition, analysis, and interpretation of data, and

drafting the article. Martin Girard and Andre Y. Denault contributed

to all aspects of this manuscript, including conception and design;

acquisition, analysis, and interpretation of data, and drafting the

article. Georges Desjardins contributed to the conception and design

of the manuscript.

Editorial responsibility This submission was handled by Dr.

Hilary P. Grocott, Editor-in-Chief, Canadian Journal of Anesthesia.

References

1. Lichtenstein DA. Lung ultrasound in the critically ill. Ann

Intensive Care 2014; 4: 1.

Transesophageal lung ultrasonography 1275

123

2. Volpicelli G, Elbarbary M, Blaivas M, et al. International

evidence-based recommendations for point-of-care lung

ultrasound. Intensive Care Med 2012; 38: 577-91.

3. Orihashi K, Hong YW, Chung G, Sisto D, Goldiner PL, Oka Y.

New applications of two-dimensional transesophageal

echocardiography in cardiac surgery. J Cardiothorac Vasc

Anesth 1991; 5: 33-9.

4. Swenson JD, Bull DA. Intraoperative diagnosis and treatment of

pleural effusion based on transesophageal echocardiographic

findings. Anesth Analg 1999; 89: 309-10.

5. Tsubo T, Sakai I, Suzuki A, Okawa H, Ishihara H, Matsuki A.

Density detection in dependent left lung region using

transesophageal echocardiography. Anesthesiology 2001; 94:

793-8.

6. Tsubo T, Yatsu Y, Suzuki A, et al. Daily changes of the area of

density in the dependent lung region—evaluation using

transesophageal echocardiography. Intensive Care Med 2001;

27: 1881-6.

7. Tsubo T, Yatsu Y, Okawa H, Ishihara H, Matsuki A.

Transesophageal echocardiography is a sensitive method to

evaluate pleural effusion. Anesthesiology 2002; 96: A322.

8. Tsubo T, Yatsu Y, Tanabe T, Okawa H, Ishihara H, Matsuki A.

Evaluation of density area in dorsal lung region during prone

position using transesophageal echocardiography. Crit Care Med

2004; 32: 83-7.

9. Verhaeghen D, Poelaert J, Ama R, Roosens C, Tempe DK,

Chaney MA. Case 2-2005: evaluation of the lungs via

transesophageal echocardiography. J Cardiothorac Vasc Anesth

2005; 19: 242-9.

10. Harasawa K, Maruyama T, Morimoto Y. Life-saving detection of

right hemothorax by transesophageal echocardiography after

femorofemoral bypass. J Cardiothorac Vasc Anesth 2006; 20:

229-31.

11. Capper SJ, Ross JJ, Sandstrom E, Braidley PC, Morgan-Hughes

NJ. Transoesophageal echocardiography for the detection and

quantification of pleural fluid in cardiac surgical patients. Br J

Anaesth 2007; 98: 442-6.

12. Yatsu Y, Tsubo T, Ishihara H, Nakamura H, Hirota K. A new

method to estimate regional pulmonary blood flow using

transesophageal echocardiography. Anesth Analg 2008; 106:

530-4.

13. Howard A, Jackson A, Howard C, Spratt P. Estimating the

volume of chronic pleural effusions using transesophageal

echocardiography. J Cardiothorac Vasc Anesth 2011; 25: 229-32.

14. Ross JJ, Braidley PC, Morgan-Hughes NJ. TEE for estimating

pleural effusion volumes. J Cardiothorac Vasc Anesth 2011; 25:

e52.

15. Rehfeldt KH, Bruggink SM, Pulido JN. Transesophageal

echocardiographic imaging of ultrasound lung rockets.

Anesthesiology 2014; 121: 1335.

16. Hilberath JN, Oakes DA, Shernan SK, Bulwer BE, D’Ambra MN,

Eltzschig HK. Safety of transesophageal echocardiography. J Am

Soc Echocardiogr 2010; 23: 1115-27; quiz 1220-1.

17. Rantanen NW. Diseases of the thorax. Vet Clin North Am Equine

Pract 1986; 2: 49-66.

18. Lichtenstein DA, Lascols N, Prin S, Meziere G. The, ‘‘lung

pulse’’: an early ultrasound sign of complete atelectasis. Intensive

Care Med 2003; 29: 2187-92.

19. Lichtenstein DA, Meziere GA, Lagoueyte JF, Biderman P,

Goldstein I, Gepner A. A-lines and B-lines: lung ultrasound asa bedside tool for predicting pulmonary artery occlusion pressure

in the critically ill. Chest 2009; 136: 1014-20.

20. Lichtenstein DA. Lung Ultrasound in the Critically Ill: The BLUE

Protocol. Switzerland: Springer International Publishing; 2015 .

21. Reub J. Sonographic imaging of the pleura: nearly 30 years

experience. Eur J Ultrasound 1996; 3: 125-39.

22. Lichtenstein D, Meziere G, Seitz J. The dynamic air

bronchogram. A lung ultrasound sign of alveolar consolidation

ruling out atelectasis. Chest 2009; 135: 1421-5.

23. Lichtenstein D, Meziere G, Biderman P, Gepner A, Barre O. The

comet-tail artifact. An ultrasound sign of alveolar-interstitial

syndrome. Am J Respir Crit Care Med 1997; 156: 1640-6.

24. Copetti R, Soldati G, Copetti P. Chest sonography: a useful tool

to differentiate acute cardiogenic pulmonary edema from acute

respiratory distress syndrome. Cardiovasc Ultrasound 2008; 6:

16.

25. Jambrik Z, Gargani L, Adamicza A, et al. B-lines quantify the

lung water content: a lung ultrasound versus lung gravimetry

study in acute lung injury. Ultrasound Med Biol 2010; 36: 2004-

10.

26. Shyamsundar M, Attwood B, Keating L, Walden AP. Clinical

review: the role of ultrasound in estimating extra-vascular lung

water. Crit Care 2013; 17: 237.

27. Denault A, Ferraro P, Couture P, et al. Transesophageal

echocardiography monitoring in the intensive care department:

the management of hemodynamic instability secondary to

thoracic tamponade after single lung transplantation. J Am

Society Echocardiogr 2003; 16: 688-92.

28. Lichtenstein D, Meziere G, Biderman P, Gepner A. The comet-

tail artifact: an ultrasound sign ruling out pneumothorax.

Intensive Care Med 1999; 25: 383-8.

29. Lichtenstein D, Meziere G, Biderman P, Gepner A. The, ‘‘lung

point’’: an ultrasound sign specific to pneumothorax. Intensive

Care Med 2000; 26: 1434-40.

30. Bouhemad B, Mongodi S, Via G, Rouquette I. Ultrasound for

‘‘lung monitoring’’ of ventilated patients. Anesthesiology 2015;

122: 437-47.

31. Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby JJ.

Bedside ultrasound assessment of positive end-expiratory

pressure-induced lung recruitment. Am J Respir Crit Care Med

2011; 183: 341-7.

32. Kim WY, Suh HJ, Hong SB, Koh Y, Lim CM. Diaphragm

dysfunction assessed by ultrasonography: influence on weaning

from mechanical ventilation. Crit Care Med 2011; 39: 2627-30.

33. Soummer A, Perbet S, Brisson H, et al. Ultrasound assessment of

lung aeration loss during a successful weaning trial predicts

postextubation distress. Crit Care Med 2012; 40: 2064-72.

34. Moschietto S, Doyen D, Grech L, Dellamonica J, Hyvernat H,

Bernardin G. Transthoracic echocardiography with Doppler

tissue imaging predicts weaning failure from mechanical

ventilation: evolution of the left ventricle relaxation rate during

a spontaneous breathing trial is the key factor in weaning

outcome. Crit Care 2012; 16: R81.

35. Lemaire F, Teboul JL, Cinotti L, et al. Acute left ventricular

dysfunction during unsuccessful weaning from mechanical

ventilation. Anesthesiology 1988; 69: 171-9.

36. Seneff MG, Zimmerman JE, Knaus WA, Wagner DP, Draper EA.

Predicting the duration of mechanical ventilation. The importance

of disease and patient characteristics. Chest 1996; 110: 469-79.

37. Caltabeloti F, Monsel A, Arbelot C, et al. Early fluid loading in

acute respiratory distress syndrome with septic shock deteriorates

lung aeration without impairing arterial oxygenation: a lung

ultrasound observational study. Crit Care 2014; 18: R91.

1276 Y. A. Cavayas et al.

123